ISSN 0102-695X
http://dx.doi.org/10.1590/S0102-695X2012005000132 Received 29 Aug 2012 Accepted 5 Oct 2012 Available online 16 Nov 2012
radical scavenging potential
Emna Faleh,
1Andreia P. Oliveira,
*,2Patrícia Valentão,
2Ali
Ferchichi,
1Branca M. Silva,
3Paula B. Andrade
21Dry Land Farming and Oasis Cropping Laboratory, Institute of Arid Regions,
Medenine, Tunisia,
2REQUIMTE/Laboratório de Farmacognosia, Departamento de Química, Faculdade
de Farmácia, Universidade do Porto, Portugal,
3Centro de Investigação em Ciências da Saúde, Universidade da Beira Interior,
Portugal.
Abstract: Ficus carica L., Moraceae, is one of the i rst plants that were cultivated by
humans, being the fruit an important crop worldwide for dry and fresh consumption. In this work, phenolics and antioxidant potential of dried fruits of seventeen Tunisian
F. carica varieties, from green, red and black phenotypes, were assessed for the i rst
time. HPLC-DAD analysis was performed. All samples presented a similar qualitative proi le. The phenolics content ranged between 29.18 and 55.56 mg/kg (in black and red phenotypes, respectively) and quercetin-3-O-rutinoside was always the major
compound. The antioxidant potential against DPPH•, superoxide and nitric oxide radicals of three varieties representing each phenotype was checked. All samples exhibited activity against the i rst two radicals in a concentration-dependent way,
“Bayoudi” variety being the most effective one (IC25 values of 10.32 and 2.89 µg/ mL, respectively). Nevertheless, only “Hammouri” variety presented some capacity to scavenge nitric oxide radical. Our results reveal nice perspectives for these typical fruits, as they present an interesting phenolic composition and good antiradical activity and may encourage their consumption for health protection.
Keywords:
antioxidant
Ficus carica L. phenolic compounds phenotypes
Introduction
The common edible i g (Ficus carica L.), belonging to the Moraceae family, has been cultivated
since ancient times. In Tunisia, i g plantations are widespread over the country and cover different climates and soils (Mars, 1995). The crop has an essential role in the development of many areas, especially those with arid or semi-arid climate (Oukabli, 2003). The fruit can
be consumed fresh, dried and canned, being an interesting source of carbohydrates, essential amino acids, vitamins A, B1, B2 and C and minerals (Solomon et al., 2006).
Additionally, i gs contain relatively high amounts of crude i bres and polyphenols, which represent 1230 and
360 mg/100 g in the dried form, respectively (Vinson et al., 2005; Solomon et al., 2006).
The drying processing of some fruits and
vegetables is one of the oldest forms of preservation.
The main purpose in drying foods is the reduction of moisture/water activity to a level which allows safe
storage over an extended period. On the other hand, it
enables a substantial reduction in weight and volume,
minimizing packaging, storage and transportation costs (Okos et al., 1992). Sun-drying is a traditional method used to obtain dried i gs, requiring low capital and simple equipment. This method produces i gs with good l avour
and consistency (Piga et al., 2004).
Phenolic compounds are secondary metabolites
quite widespread in nature. Despite this almost ubiquity,
experimental evidence has demonstrated that some of
them can work as useful markers of the botanical origin of several plant food products (wine, coffee beans, and jams) (Spanos & Wrolstad, 1992). Additionally, within
each species, the nature of these compounds can vary from organ to organ and several other factors can contribute to the variability in the phenolic composition, such as cultivar and genetics, geographical origin, maturity, climate, position on tree, agricultural practices, industrial
processing and storage conditions (Spanos & Wrolstad, 1992). These compounds have demonstrated a wide range
of important biological effects, including antioxidant,
anti-carcinogenic, anti-atherogenic, anti-inl ammatory,
and antimicrobial activities (García-Alonso et al., 2004; Yildirim, 2006).
Some studies have been performed in dried igs to characterize the presence of mycotoxins (Karaca &
Nas, 2008), to describe several morphological, chemical and sensorial alterations occurring during the drying
process (Piga et al., 2004; Aljane & Ferchichi, 2007; Aljane et al., 2008) and to determine their total phenolic
content and antioxidant potential (Vinson et al., 2005).
However, to our knowledge there is no report concerning phenolics proile and antioxidant capacity of the most abundant ig varieties in southern Tunisia, where several phenotypes are found: “Zidi”, “Sawoudi”, “Magouli-ekchine”, “Hami” and “Kahli” correspond to black varieties, “Bayoudi”, “Besbassi”, “Bither”, “Makbech”,
“Chaâri”, “Magouli” and “Naasan” are green ones,
while “Minouri”, “Hamouri”, “Ragoubi”, “Weldeni” and
“Croussi” are red.
Interest in fruits as source of natural antioxidants prompted us to investigate the phenolic constituents of
F. carica dried fruits. So, the work herein represents a
contribution to the knowledge of the seventeen Tunisian ig varieties from the distinct phenotypes above referred. Thus, their phenolic proile was determined by HPLC coupled to diode array detector (HPLC-DAD). Their antioxidant potential was also studied, by evaluating their 2,2-diphenyl-1-picrylhydrazyl radical (DPPH•), nitric
oxide and superoxide scavenging properties.
Materials and Methods
Plant material
Fig trees Ficus carica L., Moraceae were grown
in the implementation area of Institute of Arid Regions
(IRA), located in Medenine, southern Tunisia. Fruits from
seventeen varieties, grouped according to the phenotype
(black, green and red), were collected in August 2008 (Table 1). Identiication was performed by Ali Ferchichi, Ph.D. (IRA). The drying process took place at IRA. The fruits were arranged in a single layer on a plate, in a greenhouse made with tulle that allowed receiving direct sunlight and protected against insects. The ambient temperature under
the tulle greenhouse, during one typical day of the drying
period, luctuated between 29 and 40° C and the maximum values were reached between 10 am and 4 pm. During the night the fruits were kept in the laboratory, at room temperature, to avoid receiving the night humidity. The igs were considered dried when the moisture content was lower than 25 % (from 6 to 15 days), which was determined by the loss in mass measured following AOAC oficial method 934.06 (AOAC, 1990). Dried samples were then kept in a desiccator, in the dark.
Standards and reagents
Quercetin-3-O-rutinoside, quercetin and ferulic
acid were from Sigma-Aldrich (St. Louis, MO, USA)
and 5-O-caffeoylquinic acid was from Extrasynthése
(Genay, France). N-(1-Naphthyl)ethylene-diamine dihydrochloride, phosphoric acid, methanol and formic
acid were from Merck (Darmstadt, Germany). Sodium nitroprusside dehydrate, sulphanilamide, β-nicotinamide
adenine dinucleotide (NADH), nitroblue tetrazolium
chloride (NBT), phenazine methosulphate (PMS) and DPPH• were obtained from Sigma-Aldrich (St. Louis, MO, USA). The water was treated in a Milli-Q water puriication system (Millipore, Bedford, MA, USA). The Chromabond C18 SPE columns (70 mL / 10000 mg) were
purchased from Macherey-Nagel (Duren, Germany).
Extracts preparation
Dried igs were triturated in a commercial mill
(Moulinex®), homogenised and approximately ca. 5 g of each sample was mixed with 100 mL of acid water (pH 2 with HCl) with magnetic stirring (300 rpm), for 15 min. The obtained solution was iltered through a
Büchner funnel, under vacuum, and then passed through
an SPE C18 column, previously conditioned with 30 mL of methanol and 70 mL of acid water. The phenolic compounds retained in the column were eluted with 40 mL of methanol. Afterwards, this solution was evaporated
to dryness under reduced pressure (40 ºC) and the dried
extract was kept at -20 °C, in the dark, until analysis.
HPLC-DAD for phenolic proile determination
Each extract was redissolved in methanol, iltered and 20 µL were analysed on an analytical HPLC
unit (Gilson), using a Spherisorb ODS2 (25.0 x 0.46 cm;
5 µm, particle size) column, applying an identiication
methodology already validated and applied for other matrices, including F. carica materials (Silva et al., 2001,
2002; Oliveira et al., 2012). Detection was achieved with
a Gilson Diode Array Detector (DAD). Spectral data from
all peaks were accumulated in the range 200-400 nm. The identity of 3-O-caffeoylquinic acid was conirmed
by comparing its chromatographic behavior and spectral
characteristics with those of 3-O-caffeoylquinic acid
obtained before by our group by transesteriication of
5-O-caffeoylquinic acid using tetramethylammonium
hydroxide (Silva et al., 2002) and those observed by us for the same compound in Cydonia oblonga Miller and
F. carica fresh fruits using the same analytical conditions
(Silva et al., 2002; Oliveira et al., 2009). The data were processed on Unipoint System software (Gilson Medical Electronics, Villiers le Bel, France). Phenolic compounds quantiication was achieved by the absorbance recorded in
the chromatograms relative to external standards. Phenolic
acids were determined at 320 nm and lavonoids at 350
and as it is an isomer of 5-O-caffeoylquinic acid, with the
same molecular weight and UV spectrum, it was quantiied
as 5-O-caffeoylquinic acid. The other compounds were
determined as themselves.
Statistical Analysis
The evaluation of statistical signiicance was determined by a paired t-test (p<0.05). Principal
component analysis (PCA) was carried out using XLSTAT 2011.2 software.
Antioxidant activity
The antioxidant activity was assessed with
“Zidi” (ZID), “Bayoudi” (BYD) and “Hamouri” (HAM)
varieties, which were chosen as representatives of black, green and red phenotypes, respectively (Table 1), because they are the most commonly consumed ones in Tunisia.
DPPH• scavenging activity
Antiradical activity was determined
spectrophotometrically in a Multiskan Ascent plate reader (Thermo; electron corporation), by monitoring the disappearance of DPPH• at 515 nm, according to a
described procedure (Oliveira et al., 2009).
Nitric oxide scavenging activity
The nitric oxide scavenging capacity was determined in a Multiskan Ascent plate reader, according
to a described procedure (Oliveira et al., 2009), based on
the reaction with Griess reagent.
Superoxide radical scavenging activity
Superoxide radicals were generated by the
NADH/PMS system and the effect of the extracts
on radical-induced reduction of NBT was monitored spectrophotometrically in a Multiskan Ascent plate
reader, as reported by Valentão et al. (2001).
Results and Discussion
Phenolic compounds
Tunisian igs were characterized by the presence of ive phenolic compounds, which were already
described in fruits and leaves of other varieties: three hydroxycinnamic acids (3-O- and 5-O-caffeoylquinic
acids and ferulic acid) (Veberic et al., 2008; Oliveira et
al., 2009; Vallejo et al., 2012), one lavonol glycoside (quercetin-3-O-rutinoside) (Oliveira et al., 2009;
Veberic et al., 2008; Vallejo et al., 2012) and one free
lavonol (quercetin) (Vaya & Mahmood, 2006) (Figures 1 and 2 and Table 1). Quantitatively, varieties from the red phenotype show a tendency for having the highest amounts of phenolic compounds and those from black the lower ones (Table 1). However, within each phenotype, the several varieties do not exhibit the same quantitative proile, which may be related with their genetic diversity (Harris & Karmas, 1975). For example, there are green varieties, such as NAAS, MAG, MKH and BYD with higher phenolics content than red ones (HAM) (Table 1). The same is observed with some black phenotype varieties (Table 1). These facts seem to suggest that, in a general way, the phenolic composition does not allow
distinguishing the three phenotypes.
Figure 1. HPLC-DAD phenolic proile of “Zidi” variety.
Detection at 320 nm. Peaks: 1, 3-O-caffeoylquinic acid; 2, 5-
O-caffeoylquinic acid; 3, ferulic acid; 4, quercetin-3-O-rutinoside;
5, quercetin.
3-C QA
5-C QA
Feru lic a
cid Q-3
-Rut
Que rcet
in
0 2 4 10 20 30 40
%
Figure 2. Phenolic proile (%) of Tunisian igs. 3-CQA, 3-
O-Caffeoylquinic acid; 5-CQA, 5-O-caffeoylquinic acid; Q-3-Rut,
quercetin-3-O-rutinoside.
In a recent study, Vallejo et al. (2012) determined the phenolic proile of dried igs of three cultivars by HPLC-MS, quercetin-3-O-rutinoside being reported as
the main metabolite. Our results agree with this, once this compound represents ca. 59-93% of total phenolics (Table 1). The same was observed in fresh F. carica fruits of other
varieties (Oliveira et al., 2009; Veberic et al., 2008; Vallejo
1 2
3
4
5 0.6
0.4
et al., 2012). On the other hand, with the exceptions of
5-O-caffeoylquinic acid and quercetin-3-O-rutinoside,
the other phenolic compounds found in our varieties were different from those described by Vallejo et al. (2012). In addition, our varieties presented a slightly lower total phenolic content (Table 1) when compared with other dried cultivars (Vinson et al., 2005; Vallejo et al., 2012).
The phenolic compounds described above
are important in the human nutrition context and,
consequently, their bioavailability has been widely
studied. Some reports have described that quercetin, 5-O
-caffeoylquinic and ferulic acids are quickly absorbed in their intact form, whereas quercetin-3-O-rutinoside
shows a slow absorption (Karakaya, 2004; Lafay & Gil-Izquierdo, 2008).
To assess the variation of the phenolic composition within Tunisian F. carica fruits, PCA was
performed on the obtained data. Figure 3 shows the projection of chemical variables, grouped by phenolic
compounds in all varieties, into the plane composed by the
Table 1. Phenolic composition of dried Tunisian Ficus carica varieties (mg/kg)a.
Varieties b 3-CQA 5-CQA Ferulic acid Q-3-Rut Quercetin Σ
Black phenotype
MAG-k nq 0.52 ± 0.06 0.64 ± 0.06 20.00 ± 0.55 0.35 ± 0.01 21.51
SWD 4.52 ± 0.16 0.40 ± 0.02 0.48 ± 0.01 39.60 ± 0.43 0.75 ± 0.01 45.75
ZID 0.34 ± 0.02 0.23 ± 0.02 1.79 ± 0.10 23.10 ± 1.53 0.21 ± 0.05 25.67
HAMI 1.08 ± 0.01 2.00 ± 0.12 2.83 ± 0.01 24.50 ± 0.16 0.72 ± 0.06 31.13
KAH 0.47 ± 0.01 0.82 ± 0.01 2.25 ± 0.05 17.50 ± 0.07 0.81 ± 0.01 21.85
Mean 1.28 0.79 1.60 24.94 0.57 29.18
SD 1.86 0.71 1.02 8.63 0.27 10.04
Max 4.52 2.00 2.83 39.60 0.81 45.75
Min 0.34 0.23 0.48 17.50 0.35 21.51
Green phenotype
NAAS 8.44 ± 0.12 0.36 ± 0.13 1.93 ± 0.96 37.50 ± 2.69 1.38 ± 0.13 49.61
CHA 0.13 ± 0.01 0.12 ± 0.01 1.33 ± 0.02 5.22 ± 0.07 0.11 ± 0.01 6.91
MAG 1.03 ± 0.01 1.15 ± 0.35 5.88 ± 0.21 24.20 ± 1.49 0.45 ± 0.01 32.71
BTH 0.34 ± 0.01 0.50 ± 0.05 0.60 ± 0.04 4.33 ± 0.07 0.42 ± 0.01 6.19
BES 3.26 ± 0.25 0.59 ± 0.01 1.62 ± 0.07 8.06 ± 0.06 0.10 ± 0.02 13.63
BYD 0.17 ± 0.03 2.56 ± 0.02 1.50 ± 0.04 55.50 ± 7.85 1.90 ± 0.14 61.68
MKH 0.14 ± 0.01 1.94 ± 0.04 1.13 ± 0.09 45.00 ± 2.52 1.43 ± 0.02 49.79
Mean 1.93 1.03 1.98 23.63 0.66 31.50
SD 3.08 0.91 1.76 20.11 0.71 22.87
Max 8.44 2.56 5.88 55.50 1.90 61.68
Min 0.13 0.12 0.60 4.33 0.10 6.19
Red phenotype
RGB nq 2.38 ± 0.52 5.56 ± 0.02 69.50 ± 5.46 0.70 ± 0.05 78.14
CRS 3.06 ± 0.10 1.04 ± 0.13 3.38 ± 0.04 50.30 ± 2.14 8.76 ± 1.89 66.54
HAM 0.06 ± 0.01 0.18 ± 0.01 1.33 ± 0.03 12.30 ± 0.76 0.35 ± 0.04 14.22
WLD 0.17 ± 0.02 1.67 ± 0.01 0.23 ± 0.01 20.50 ± 0.08 0.12 ± 0.01 22.69
MIN 1.65 ± 0.15 2.13 ± 0.06 1.44 ± 0.11 88.40 ± 3.84 2.58 ± 0.24 96.20
Mean 0.99 1.48 2.39 48.20 2.50 55.56
SD 1.35 0.89 2.10 32.13 3.63 35.61
Max 3.06 2.38 5.56 88.40 8.76 96.20
Min 0.06 0.18 0.23 12.30 0.12 14.22
aValues are expressed as mean±standard deviation of three assays; nq, not quantiied; Σ, sum of the determined phenolic compounds; 3-CQA, 3-O
-caffeoylquinic acid; 5-CQA, 5-O-caffeoylquinic acid and Q-3-rut, quercetin-3-O-rutinoside. b MAG-k, “Magouli-Ekchine”; SWD, “Sawoudi”; ZID,
principal axes F1 and F2 containing 68.89% of the total variance. We can observe that NAAS (green phenotype),
CRS and MIN (red phenotypes) are positively correlated to their higher concentrations of 3-O-caffeoylquinic acid,
quercetin and quercetin-3-O-rutinoside, respectively.
HAMI (black phenotype), MKH, MAG, BYD (green phenotypes) and RGB (red phenotype) are projected into
the plane formed by F1 positive axis and F2 negative axis
due to their low amounts of 3-O-caffeoylquinic acid and
quercetin. In contrast, the other varieties are presented
into the planes formed by F1 and F2 negative axes,
corresponding to the samples with lower quantities of all phenolic compounds. These results conirmed that the phenolic composition does not allow to distinguish the several Tunisian F. carica phenotypes, since all varieties are composed by the same compounds, at similar amounts,
with no signiicant differences between them.
Antioxidant activity
The DPPH• assay provides basic information on the antiradical activity of extracts (Fukumoto & Mazza, 2000). The extracts of the representative phenotypes exhibited DPPH• scavenging capacity, in a concentration-dependent way (Figure 4A), BYD and HAM being the most effective varieties (Table 2).
The different samples also revealed superoxide scavenging ability, which was concentration-dependent
(Figure 4B), BYD being the most active against this free
radical (Table 2). Superoxide radical is one of the most
effective free radicals that can arise from physiological processes, such as purine metabolism (Borges et al.,
2002) or electron leakage from the respiratory chain that will reduce oxygen (Halliwel, 1991). Although necessary
in many physiological processes, its augmentation can be in the genesis of several pathological conditions
(Halliwel, 1991), such as cell damage in cardiovascular
and neurological systems and inactivation of enzymes and other proteins by oxidation and nitration (Pacher et
al., 2007).
In what concerns to nitric oxide, HAM was
the only variety displaying a protective effect, having
an inhibitory capacity of ca. 30% for the highest tested concentration (1.67 mg/mL). Nitric oxide exerts
important biological functions, including blood pressure control, neural signal transduction and antimicrobial protection (Ignarro, 1999). Nevertheless, this nitrogen reactive species can be responsible for oxidative damage,
once it reacts rapidly with superoxide radical to form peroxynitrite, a major damaging oxidant produced in vivo
(Beckman, 1996).
The high scavenging capacity veriied with the
variety chosen from the green phenotype (BYD) can
be, at least partially, related with its higher phenolic content (Tables 1 and 2). On the other hand, although ZID variety presented higher quantities of phenolics than HAM (Table 1), it had lower antioxidant capacity (Table 2). This might be explained by the existence of possible Figure 3. PCA of all phenolic compounds in Tunisian Ficus carica fruits: projection of phenolic compounds (variables: 3-CQA, 3-O-caffeoylquinic acid; 5-CQA, 5-O-caffeoylquinic acid; ferulic acid; Q-3-Rut, quercetin-3-O-rutinoside; quercetin;
BES, “Besbassi”; BTH, “Bither”; SWD, “Sawoudi”; WLD, “Weldeni”; ZID, “Zidi”; BYD, “Bayoudi”; MAG-k, “Magouhi-Ekchine”; HAMI, “Hami”; MIN, “Minouri”; KAH, “Kahli”; MKH, “Makbech”; CHA, “Chaâri”; HAM, “Hamouri”; RGB,
“Ragoubi”; CRS, “Croussi”; MAG, “Magouli”; NAAS, “Naasan”) into the plane composed by the principal axes F1 and F2
(68.89%).
3-CQA
5-CQA Ferulic acid Q-3-Rut Quercetin
-1 -0,75 -0,5 -0,25 0 0,25 0,5 0,75 1
-1 -0,75 -0,5 -0,25 0 0,25 0,5 0,75 1
F2 (25.24 %)
F1 (43.65 %) Variables (axes F1 and F2: 68.89 %)
MAG-k SWD
ZID
NAAS
CHA
MAG HAM
BES
HAMI BTH
RGB WLD
CRS
KAH
MIN
BYD MKH
-2 -1 0 1 2 3
-4 -3 -2 -1 0 1 2 3
F2 (25.24 %)
F1 (43.65 %)
interactions between phenolics and other compounds
present in the tested extract and not determined herein,
namely antagonisms, which may result in the decrease of
activity.
Overall, the results obtained in the different assays revealed F. carica dried figs good capacity to
scavenge free radicals. This ability is likely to be partially
related to the presence of phenolic compounds, since they are recognized as able to act as antioxidants by
different ways: as reducing agents, hydrogen donators, free radicals scavengers, and singlet oxygen quenchers and, therefore, as cell saviours (Halliwell et al., 2000; Fattouch et al., 2007). Additionally, these compounds are known to inhibit some enzymes involved in radical generation (Parr & Bolwell, 2000) and to up-regulate endogenous antioxidant enzymes (Zhan & Yang,
2006). In fact, our research group has demonstrated the strong antioxidant activity of several natural extracts
characterized by high contents of quercetin-3-O -rutinoside as these ones, namely those obtained from
Cydonia oblonga Mill., Dracaena draco (L.) L. or
Lycopersicon esculentum Mill. (Oliveira et al., 2010; Ferreres et al., 2010; Silva et al., 2011; Santos et al.,
2011). Furthermore, we can also highlight the presence
of 5-O-caffeoylquinic and ferulic acids and quercetin,
which are known to be excellent in vitro antioxidants,
namely against DPPH•, nitrogen and oxygen reactive species (Rice-Evans et al., 1996, 1997; Cai et al., 2004; Boots et al., 2008). On the other hand, as we referred above, we cannot ignore the existence of other non-determined compounds with antioxidant activity, such
as those resulting from Maillard reaction (Billaud et al., 2005).
Conclusion
This is the irst study involving these ig varieties and contributes to the knowledge of their
phenolic composition and antioxidant properties. A
similar qualitative phenolic proile was observed and the data obtained indicate that, in a general way, phenolics
composition does not depend on the phenotype or the
variety. Dried igs revealed good antiradical capacity against DPPH• and O2
•-, which might be partially explained by their phenolic compounds. Thus, the consumption of these dried igs in a balanced diet may provide beneicial
health effects.
Table 2. IC25 values of dried Tunisian F. carica varieties
obtained in antioxidant activity evaluation assays (μg/mL)a.
Assay Variety
HAM BYD ZID
DPPH• 14.12±4.72a 10.32±0.58a 155.19±14.56b
O2•- 14.00±2.09a 2.89±0.94b 100.69±20.97c
aIn the same line, means with different letter are signiicantly different
(p<0.05).
Acknowledgment
The authors are grateful to Fundação para a Ciência e a Tecnologia for grant no. PEst-C/EQB/ LA0006/2011 and to Programa COMPETE (PEst-C/ SAU/UI0709/2011). APO (SFRH/BD/47620/2008) is indebted to FCT for the grant.
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*Correspondence
Andreia P. Oliveira
REQUIMTE/Laboratório de Farmacognosia, Departamento de Química, Faculdade de Farmácia, Universidade do Porto
Rua de Jorge Viterbo Ferreira, nº 228, 4050-313 Porto, Portugal
